Dataset Information

Blue light promotes zero-valent sulfur production in a deep-sea bacterium.

ABSTRACT: Increasing evidence has shown that light exists in a diverse range of deep-sea environments. We unexpectedly found that blue light is necessary to produce excess zero-valent sulfur (ZVS) in Erythrobacter flavus 21-3, a bacterium that has been recently isolated from a deep-sea cold seep. E. flavus 21-3 is able to convert thiosulfate to ZVS using a novel thiosulfate oxidation pathway comprising a thiosulfate dehydrogenase (TsdA) and a thiosulfohydrolase (SoxB). Using proteomic, bacterial two-hybrid and heterologous expression assays, we found that the light-oxygen-voltage histidine kinase LOV-1477 responds to blue light and activates the diguanylate cyclase DGC-2902 to produce c-di-GMP. Subsequently, the PilZ domain-containing protein mPilZ-1753 binds to c-di-GMP and activates TsdA through direct interaction. Finally, Raman spectroscopy and gene knockout results verified that TsdA and two SoxB homologs cooperate to regulate ZVS production. As ZVS is an energy source for E. flavus 21-3, we propose that deep-sea blue light provides E. flavus 21-3 with a selective advantage in the cold seep, suggesting a previously unappreciated relationship between light-sensing pathways and sulfur metabolism in a deep-sea microorganism.

SUBMITTER: Cai R

PROVIDER: S-EPMC10267690 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Blue light promotes zero-valent sulfur production in a deep-sea bacterium.

Cai Ruining R He Wanying W Zhang Jing J Liu Rui R Yin Ziyu Z Zhang Xin X Sun Chaomin C

The EMBO journal 20230322 12

Increasing evidence has shown that light exists in a diverse range of deep-sea environments. We unexpectedly found that blue light is necessary to produce excess zero-valent sulfur (ZVS) in Erythrobacter flavus 21-3, a bacterium that has been recently isolated from a deep-sea cold seep. E. flavus 21-3 is able to convert thiosulfate to ZVS using a novel thiosulfate oxidation pathway comprising a thiosulfate dehydrogenase (TsdA) and a thiosulfohydrolase (SoxB). Using proteomic, bacterial two-hybri ...[more]

PMID: 36946144

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Project description:Light is a ubiquitous energy source and environmental signal that broadly impacts the lifestyle of a large number of photosynthetic/nonphotosynthetic microorganisms living in the euphotic layer. However, the responses of deep-sea microbes to light are largely unknown, even though blue light is proposed to be distributed in the deep ocean. Here, we successfully cultured a novel bacterial species, named Spongiibacter nanhainus CSC3.9, from deep-sea cold seep samples by a blue light induction approach. The growth of strain CSC3.9 was obviously promoted by the illumination of blue light. We next determined BLUF (a typical blue light photoreceptor) was the most essential factor directing light sensing of strain CSC3.9 through a combined proteomic and genetic method. The function of light sensing mediated by BLUF was further confirmed by the in vitro-synthesized protein. Notably, homologs of BLUF widely existed across the marine microorganisms (containing Spongiibacter species) derived from different environments, including cold seeps. This strongly indicates that the distribution of light utilization by the nonphototrophic bacteria living in the ocean is broad and has been substantially underestimated. IMPORTANCE Extensive studies have been conducted to explore the mechanisms of light sensing and utilization by microorganisms that live in the photic zone. Strikingly, accumulated evidence shows that light is distributed in the deep biosphere. However, the existence and process of light sensing and utilization by microbes inhabiting the deep ocean have been seldom reported. In the present study, a novel bacterial strain, Spongiibacter nanhainus CSC3.9, was enriched and purified from a deep-sea cold seep sample through a blue light induction method. Combined with genomic, proteomic, genetic, and biochemical approaches, the mechanism of this novel strain sensing blue light through a BLUF-dependent pathway was detailed. Our study provides a good model to study the mechanisms of light sensing mediated by deep-sea nonphototrophic bacteria.

Project description:Zero-valent sulfur (ZVS) distributes widely in the deep-sea cold seep, which is an important immediate in the sulfur cycle of cold seep. In our previous work, we described a novel thiosulfate oxidation pathway determined by thiosulfate dehydrogenase (TsdA) and thiosulfohydrolase (SoxB) mediating the conversion of thiosulfate to ZVS in the deep-sea cold seep bacterium Erythrobacter flavus 21-3. However, the occurrence and ecological role of this pathway in the deep-sea cold seep were obscure. Here, we cultured E. flavus 21-3 in the deep-sea cold seep for 10 days and demonstrated its capability of forming ZVS in the in situ field. Based on proteomic, stoichiometric analyses and microscopic observation, we found that this thiosulfate oxidation pathway benefited E. flavus 21-3 to adapt the cold seep conditions. Notably, ~25% metagenomes assembled genomes derived from the shallow sediments of cold seeps contained both tsdA and soxB, where presented abundant sulfur metabolism-related genes and active sulfur cycle. Our results suggested that the thiosulfate oxidation pathway determined by TsdA and SoxB existed across many bacteria inhabiting in the cold seep and frequently used by microbes to take part in the active cold seep biogeochemical sulfur cycle. IMPORTANCE The contribution of microbes to the deep-sea cold seep sulfur cycle has received considerable attention in recent years. In the previous study, we isolated E. flavus 21-3 from deep-sea cold seep sediments and described a novel thiosulfate oxidation pathway in the laboratorial condition. It provided a new clue about the formation of ZVS in the cold seep. However, because of huge differences between laboratory and in situ environment, whether bacteria perform the same thiosulfate oxidation pathway in the deep-sea cold seep should be further confirmed. In this work, we verified that E. flavus 21-3 formed ZVS using this pathway in deep-sea cold seep through in situ cultivation, which confirmed the importance of this thiosulfate oxidation pathway and provided an in situ approach to study the real metabolism of deep-sea microorganisms.

Project description:BackgroundIonic and molecular carriers of dissolved (filter-passing) zero-valent sulfur (S0) in anaerobic natural waters include polysulfides, Sn2-, molecular S8(aq), organic macromolecules and certain higher valent thioanions. Because S0 is rapidly transferred among these various carriers, its biogeochemical roles in such processes as dehalogenation of organic compounds, chelation of trace metals, and anaerobic microbial metabolism are not determined solely by one ionic or molecular species. Here, S0 is treated collectively as a virtual thermodynamic component, and computational as well as graphical methods for quantifying its activity (aS0) in natural waters are presented. From aS0, concentrations of the ionic and molecular carriers of S0 can be calculated easily.ResultsConcentration ratios of any two polysulfide ions define aS0 (Method I). Unfortunately these concentrations are often too low in nature for accurate quantification with current methods. Measurements of total divalent sulfur (ΣS-II), zero-valent sulfur (ΣS0) and pH provide a more widely applicable approach (Method II). Systematic errors in ΣS0 measurements are the main limit to accuracy of this method at the present time. Alternative methods based on greigite solubility and potentiometry are discussed. A critical comparison of Methods I and II reveals inconsistencies at low ΣS0/ΣS-II that imply errors in the thermodynamic data for HS2- and S2-. For samples having low ΣS0/ΣS-II, an interim remedy is recommended: letting pKa2 = 6.3 for all HSn- ions.ConclusionsNewly assembled data for aS0 in a selection of anaerobic natural waters indicate that S0 is always metastable in the surveyed samples with respect to disproportionation to sulfide and sulfate. In all the surveyed environments, sulfur-rich minerals, such as greigite, covellite and orpiment, are stable in preference to their sulfur-poor cohorts, mackinawite, chalcocite and realgar. The aS0 values in the dataset span conditions favoring Hg-polysulfide complexes vs. Hg-sulfide complexes, implying that aS0 could affect Hg-methylation rates in nature. No support is found for the common assumption that aS0 = 1 in reducing natural waters. This paper calls attention to an urgent need for improved measurement methods, especially for total zero-valent sulfur, as well as new determinations of ionization constants for all HSn- species.

Dataset Information

Blue light promotes zero-valent sulfur production in a deep-sea bacterium.

Publications

Blue light promotes zero-valent sulfur production in a deep-sea bacterium.

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